Phylogenetic relationships of the pygmy rice ratsof the genus Oligoryzomys Bangs, 1900(Rodentia: Sigmodontinae)zoj_621 551..566

R. EDUARDO PALMA1*, ENRIQUE RODRÍGUEZ-SERRANO1, ERIC RIVERA-MILLA2,CRISTIAN E. HERNANDEZ3, JORGE SALAZAR-BRAVO4, MARIA I. CARMA5,SEBASTIAN BELMAR-LUCERO1, PABLO GUTIERREZ-TAPIA1, HORACIO ZEBALLOS1

and TERRY L. YATES6

1Departamento de Ecología and Centro de Estudios Avanzados en Ecología y Biodiversidad,Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago6513677, Chile2Molecular Genetic Group, Leibniz Institute for Age Research, Fritz Lipmann Institute,Beutenbergstrasse 11, 07745 Jena, Germany3Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad deConcepción, Concepción, Chile4Department of Biological Sciences, Texas Tech University, Lubbock TX 79409-3131, USA5Cátedra de Diversidad Animal II, Facultad de Ciencias Exactas y Naturales, Universidad Nacionalde Catamarca, Av. Belgrano 300, 4700 Catamarca, Argentina6Department of Biology and Museum of Southwestern Biology, University of New Mexico,Albuquerque, NM 87131-1091, USA

Received 9 February 2009; accepted for publication 31 July 2009

Sequences from two mitochondrial genes (cytochrome b and NADH1) were used to produce a molecular phylogenyfor 12 named and two undescribed species of the genus Oligoryzomys. All analyses placed Oligoryzomys microtisas the most basal taxon, a finding consistent with previous studies that suggested the west-central Amazon as acentre of origin for the tribe Oryzomyini to which Oligoryzomys belongs. Biogeographically, this suggests thatOligoryzomys had a South American origin, and later advanced northwards, entering Central America and Mexicomore recently. Different analyses have provided consistent support for several additional clades that did notnecessarily agree with the species groups hypothesized by previous studies. A molecular clock derived for these datasuggests an origin for the genus of 6.67 Mya, with most speciation within the genus occurring between 3.7 and1.5 Mya.

© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 160, 551–566.doi: 10.1111/j.1096-3642.2009.00621.x

ADDITIONAL KEYWORDS: cytochrome b – NADH1 – Neotropics – phylogeny.

INTRODUCTION

New World mice are conventionally recognized withinthe subfamily Sigmodontinae, which includes about450 species (Steppan, Adkins & Anderson, 2004;

Musser & Carleton, 2005). However, some authorsdivide this taxon into the Sigmodontinae s.s., which ispredominantly South American in distribution, withapproximately 300 species, and the almost exclusivelyNorth American Neotominae (Steppan et al., 2004).There are four major hypotheses concerning thearrival and radiation of sigmodontine rodents in*Corresponding author. E-mail: epalma@bio.puc.cl

Zoological Journal of the Linnean Society, 2010, 160, 551–566. With 4 figures

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South America: (1) sigmodontines evolved in NorthAmerica prior to 7 Mya (Upper Miocene), and reachedSouth America by waif dispersal from CentralAmerica about 6 Mya in the Upper Miocene (Mar-shall, 1979; Marshall et al., 1982); (2) sigmodontinesdifferentiated in tropical North America beforespreading to South America by overland dispersalafter the establishment of the Panamanian landbridge by Plio–Pleistocene times, about 3.5 Mya(Patterson & Pascual, 1972; Baskin, 1978; Simpson,1980; Webb, 1991); (3) South American sigmodontinesdifferentiated ‘in situ’ from an invading northernancestor arriving by over-water dispersal duringMiocene times before the Panamanian land bridge,about 8 Mya (Hershkovitz, 1966, 1972; Savage, 1974;Reig, 1980, 1981, 1986); and (4) sigmodontines differ-entiated rapidly in South America from an ancestralform arriving by overland dispersal through thealready formed Panamanian land bridge, approxi-mately 3 Mya (Simpson, 1940, 1950). The occurrenceof some fossil sigmodontine mice already differenti-ated in current genera date back to the PlioceneMontehermosan of Argentina, before the establish-ment of the Panamanian land bridge. This suggestsan earlier origin for the entrance of these taxa intoSouth America (Reig, 1981). In fact, calibrationsbased on molecular phylogeny suggest an origin ofabout 5–9 Mya (Engel et al., 1998) and 10 Mya (Spo-torno, 1986; Smith & Patton, 1999; Steppan et al.,2004). A recent classification proposed by Steppanet al. (2004) based on nuclear genes recognized a newtaxon within sigmodontines, Oryzomyalia, whichincludes important components of the South Ameri-can mouse radiation, such as the tribe Oryzomyiniand all of their related taxa. This tribe includes 28genera (Weksler et al., 2006), among which are therice rats of the genus Oligoryzomys Bangs, 1900. Thistaxon was originally included as a subgenus withinOryzomys, but Carleton & Musser (1989) recognizedOligoryzomys as a valid genus based on several mor-phological features, including cranial, tooth, andstomach morphology, as well as its reduced body size,tail longer than head and body, short and broadhindfoot, small skull, and a convex interorbital bone.In the last decade the genus Oligoryzomys has beenthe focus of epidemiologic studies, as several speciesof the genus constitute the major reservoir of Han-tavirus, which is an emerging infectious disease agentthat causes a cardiopulmonary syndrome in humans,with lethal consequences in some cases (Lee & vander Groen, 1989). Different species of Oligoryzomysare the reservoirs of different Hantavirus strains, andthey seem to constitute a coevolutionary association(Yates et al., 2002; Rivera et al., 2007). Regardingtheir habitats, Oligoryzomys species may be found ina variety of environments, from high-elevation Puna

habitat in the central Andes Mountains (Oligory-zomys andinus Osgood, 1914) to lowland tropical andsubtropical areas (Oligoryzomys eliurus Wagner, 1845and Oligoryzomys chacoensis Myers and Carleton,1981). The genus has a wide distribution in the Neo-tropics extending from Mexico (Oligoryzomys fulve-scens Saussure, 1860), through Central America(Oligoryzomys vegetus Bangs, 1902), and southwardsto Patagonia (Oligoryzomys longicaudatus Bennett,1832; Fig. 1A and B).

Tate (1932) recognized about 30 species of Oligory-zomys, whereas Hershkovitz (1966) believed that Oli-goryzomys represented a single species, with differentforms described as subspecies. Musser & Carleton(1993) recognized 15 taxa of Oligoryzomys, but recentrevisions by Musser & Carleton (2005) added threemore, giving a total of 18 species. Weksler & Bonvi-cino (2005) described two new endemic species fromBrazil (Oligoryzomys moojeni and Oligoryzomysrupestris) but, at the same time placed O. eliurus andOligoryzomys delticola (Thomas, 1917) as junior syn-onyms of Oligoryzomys nigripes (Olfers, 1818), thusthe total number of species remains the same asconsidered by Musser & Carleton (2005). Most speciesof the genus have been described based on morphol-ogy and chromosome number. In fact, most specieshave different karyotypes with 2n between 46 and 70(Andrades-Miranda et al., 2001; Weksler & Bonvicino,2005).

Little is known about the evolutionary relation-ships within Oligoryzomys. Based on morphology,Carleton & Musser (1989) concluded that the genusis a monophyletic group, and recognized 12 speciesand three undescribed forms that were placed intofive groups: the fulvescens group, including O. fulve-scens, Oligoryzomys arenalis (Thomas, 1913), and O.vegetus; the microtis group, including Oligoryzomysmicrotis (Allen, 1916); the andinus group, includingO. andinus and O. chacoensis; the flavescens group,including Oligoryzomys flavescens (Waterhouse,1837) and three undescribed species; and thenigripes group, including O. nigripes, O. eliurus, Oli-goryzomys destructor (Tschudi, 1844), O. delticola,and O. longicaudatus. Dickerman & Yates (1995)analysed the allozyme variation among selected ory-zomyine taxa, including five species of Oligoryzomys,and concluded that the genus is monophyletic. Simi-larly, based on 401-bp sequences of the mitochon-drial cytochrome b (cyt B) gene among eight speciesof the genus, Myers, Lundrigan & Tucker (1995) con-cluded that the genus was a natural group. Later,Weksler (2003) arrived at the same conclusion basedon a phylogeny of the oryzomyine rodents, usingsequences of the first exon of the IRBP nuclear genethat included five species of Oligoryzomys. Morerecently, from the results presented by Rivera et al.

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(2007) based on d-loop sequences, it is also possibleto conclude the monophyly of the genus, althoughthey evaluated only the systematic relationships ofthe species that occur in Argentina (seven taxa).Finally, a recently published study by Miranda et al.(2008) based on cyt B sequences including 12 speciesof Oligoryzomys also concluded the monophyly of thegenus. All the latter studies agreed on the mono-phyly of Oligoryzomys, but none of them recognizedthe species groups as proposed by Carleton &Musser (1989). Since then, no other study designedto evaluate the phylogenetic relationships of most ofthe currently known species of Oligoryzomys hasbeen published.

The above information suggests that Oligoryzomysis a monophyletic group. We tested this hypothesisand evaluated whether the species groups proposedby Carleton & Musser (1989) constitute naturalgroups (clades). We evaluated the phylogeny in 12species of Oligoryzomys [seven species overlappedwith those considered in Miranda’s (2008) study]. Inaddition, we included two undescribed forms: Oligo-ryzomys sp. 1 (field catalogue of one of us, MIC) andOligoryzomys sp. B (Carleton & Musser, 1989).Another major objective was to calibrate a molecularclock to hypothesize the time of origin and radiationof Oligoryzomys, and contrast those results withhypotheses about the origin and radiation of sigmo-

Figure 1A. Approximate geographic distribution of species of the genus Oligoryzomys, including undescribed taxaOligoryzomys sp. 1 and Oligoryzomys sp. B (the distribution of Oligoryzomys sp. B is according to trapping recordsreported in Carleton and Musser, 1989).

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dontines in the Neotropics. To accomplish these goals,we sequenced the cyt B and nicotinamide dinucleotidedehydrogenase subunit 1 (NADH1) mitochondrialgenes in 16 specimens of the 14 taxa plus two out-groups. Aligned sequences were analysed phylogeneti-cally using different optimality criteria for eachmolecular marker and for the total evidence matrix.

MATERIAL AND METHODSDNA SEQUENCING AND ALIGNMENT

DNA was extracted from frozen tissue (mainly liver)from 16 specimens: 14 Oligoryzomys species and twoout-groups (see below). Capture and handling proce-dures followed guidelines approved by the AmericanSociety of Mammalogists (Gannon et al., 2007).According to Musser & Carleton’s (2005) speciesaccount, we lack six species of Oligoryzomys, for

which samples were unavailable: a new formdescribed from Brazil, Oligoryzomys stramineus (Bon-vicino and Weksler, 1998); Oligoryzomys griseolus(Osgood, 1912) from Venezuela, of which there havebeen no recent captures (M. Aguilera to R.E. Palma,pers. comm.); Oligoryzomys victus (Thomas, 1898)from Lesser Antilles, which is presumably extinct(Musser & Carleton, 2005); Oligoryzomys magellani-cus (Bennet, 1835) (Isla Harrison, Magallanes, Chile);O. arenalis (Lambayeque, Perú), and Oligoryzomysbrendae (Massoia, 1998) (although see below). Inaddition, we could not get samples from two otherBrazilian forms: O. moojeni and O. rupestris,described by Weksler & Bonvicino (2005). DNA wasextracted according to the techniques outlined inLaird et al. (1991). In most cases we sequenced asingle specimen of each species, except for O. longi-caudatus and Oligoryzomys sp. 1 (Table 1). We

Figure 1B. Continued.

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Table 1. List of species, collection/museum numbers, localities, and GenBank accessession numbers of Oligoryzomyssequenced for the cytochrome b and NADH1 mitochondrial genes

Museum/catalog Species Locality

Cytochromeb access

NADH1access Coordinates

NK101588 O. fulvescens Panamá, Prov. Los Santos,Península de Azuero

EU 192164 EU 192190 07°46!04"S,80°17!04"W

KU142065 O. vegetus Costa Rica, Prov. PuntaArenas, Monteverde, CerroAmigos, 1760 m a.s.l.

EU 192165 EU 192189 not available

NK13425 O. microtis Bolivia, Depto Beni, 3 km SRurrenabaque, 365 m a.s.l.

EU 192172 EU 192191 14°30!S, 67°34!W

NK21532 O. flavescens Bolivia, Depto Chuquisaca,9 km by road N of Padilla,2000 m a.s.l.

EU 192170 EU 192177 19°18!S 64°22!W

NK42266 O. eliurus Brasil, Sao Paulo, DeptoGuariba

EU 192163 EU 192182 21°25!30.9"S,48°15!24.9"W

NK22846 O. destructor Bolivia, Depto Cochabamba,Tinkursiri, 17 km E ofTotora, 2950 m a.s.l.

EU 192171 EU 192176 17°45!S, 65°02!W

NK72388 O. chacoensis Paraguay, Depto Boquerón,Fortin Toledo, 600 m a.s.l.

EU 192173 EU 192183 22°01!20.3"S,60°36!2.5"W

NK11547 O. andinus Bolivia, Depto Oruro, 2 kmW of Huancaroma, 3730 ma.s.l.

AY 452200 EU 192186 17°40!S, 67°30!W

GD259 O. fornesi Paraguay, Depto Paraguarí,Costa Río Tebicuary,1.2 km aguas abajo

EU 192158 EU 192184 26°24.050S,57°02.340W

GD569 O. delticola Uruguay, Depto Rivera,Lunarejo (propiedadSr. Abelenda)

EU 192162 EU 192181 31°06!S, 55°58!W

MIC210 Oligoryzomyssp. 1

Argentina, Prov. Catamarca,Dept Ambato, Las Juntas

EU 192167 EU 192178 28°06!34"S,65°55!0"W

MIC211 Oligoryzomyssp. 1

Argentina, Prov. Catamarca,Dept Ambato, Las Juntas

EU 192168 EU 192180 28°06!34"S,65°55!0"W

MIC203 Oligoryzomyssp. 1

Argentina, Prov. Catamarca,Dept Ambato, Las Juntas

EU 192169 EU 192179 28°06!34"S,65°55!0"W

GD547 O. nigripes Paraguay, Depto Paraguarí,Costa del Río Tebuicary

EU 192161 EU 192175 26°30.816S,57°14.444W

MUSA2625 Oligoryzomyssp. B 3203

Perú, Depto Puno, Prov.Sandia, Distrito Limbani,Pueblo de Limbani

EU 192159 EU 192185 not available

JCT1960 O. longicaudatus Chile, Magallanes, Prov.Antarctica Chilena, IslaNavarino, Bahía Inútil

EU 192160 EU 192187 54°59!S, 68°13!W

NK95245 O. longicaudatus Chile, Aysén, Prov.Coyhaique, ForestalMininco

AY 346567 EU 192188 45°31!03"S,71°51!49"W

NK37843 Transandinomystalamancae

Ecuador, Depto El Oro, RíoPuyango

EU 192166 EU 192192 03°53!00"S,80°07!00"W

NK27671 Holochilusbrasiliensis

Bolivia, Depto Beni, SanRamón, Río Mamoré

EU 192174 EU 192193 13°16!19"S,64°37!33"W

GD, field catalogue of Guillermo D’Elía, Universidad de Concepción, Chile; JCT, field catalogue number of Juan CarlosTorres-Mura, Museo Nacional de Historia Natural, Santiago, Chile; KU, Kansas University Natural History Museum, TheUniversity of Kansas, USA; MIC, field catalogue of María Inés Carma; MUSA, Museo de la Universidad de San Agustín,Arequipa, Perú; NK, voucher reference number used for the Museum of Southwestern Biology, University of New Mexico,New Mexico, USA.

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amplified the cyt B and the NADH1 mitochondrialgenes via the polymerase chain reaction (PCR; Saikiet al., 1988) using Taq DNA Polymerase (Invitrogen)and primers L (MSB) 5!-GACATGAAAAATCATCGTTGTAATTC-3! and MVZ-14 (Smith & Patton, 1993)for the cyt B gene, and 16S.f2 5!-TACGACCTCGATGTTGGATCAGG-3! and Met.r1 5!-GGGGTATGGGCCCRARAGC-3! for the NADH1 gene. The PCRs wereperformed using the following thermal profiles. Forcyt B: 35 cycles of 94 °C denaturation for 40 s; 42 °Cannealing for 40 s; and a 72 °C extension for 1 min20 s. For NADH1: 35 cycles of 94 °C denaturation for40 s; 50 °C annealing for 35 s; and a 72 °C extensionfor 1 min 20 s. Double-stranded PCR products werepurified using QIAquick (Qiagen). Sequencing wasconducted through cycle sequencing (Murray, 1989)using the PCR primers labelled with the Big DyeTerminator kit (Perkin Elmer), and the sequencingreactions were analysed in an ABI Prism 310 auto-mated sequencer. The PCR products were sequencedat least two times to ensure sequence fidelity.Sequences were aligned by eye and using ClustalX tomaintain amino acid sequences (Thompson et al.,1997). We also used MacClade 3.08 (Maddison &Maddison, 1992) to translate nucleotide codons intoamino acids. Alignment was conducted for each dataset, as well as for the complete data matrix. Allsequences were entered into GenBank, and accessionnumbers are given in Table 1. The substitution ratewas evaluated for both genes using the best-fittingnucleotide substitution model obtained with Modelt-est (Posada & Crandall, 1998). Through this approxi-mation we demonstrated that although bothmolecular markers belong to the same genome, theyshowed different evolutionary trends (Fig. 2).

PHYLOGENETIC ANALYSES AND CLOCK CALIBRATION

Phylogenetic reconstruction was performed throughmaximum parsimony (MP) using PAUP* 4.0b10(Swofford, 2002). Both mitochondrial data sets (cyt Band NADH1) were analysed separately and as acombined data matrix. Congruence between cyt Band NADH1 data sets was tested using the partitionhomogeneity test (Farris et al., 1994) implemented inPAUP* 4.0b10 with 1000 replicates, excludinginvariant characters (Cunningham, 1997). For parsi-mony analysis we treated all characters as unor-dered with four possible states (A, C, G, and T), andwe used the characters that were phylogeneticallyinformative. As the transition/transversion (ts/tv)rate was 4 : 1 for each mitochondrial marker, weperformed weighted parsimony (WP). For WP, a heu-ristic search was performed with ten random addi-tions, and branch swapping was performed via treebisection reconnection (TBR; Nei & Kumar, 2000).

The reliability of nodes was estimated by non-parametric bootstrap (Felsenstein, 1985) after 1000pseudoreplications. Phylogenetic trees were rootedwith the out-group criterion using two oryzomyinetaxa, Holochilus brasiliensis and Transandinomystalamancae (formerly known as Oryzomys talaman-cae; Weksler, Percequillo & Voss, 2006). Holochilusbrasiliensis is part of the sister clade to which Oli-goryzomys belongs, whereas T. talamancae corre-sponds to a more distant related lineage withinOryzomyini (Weksler, 2006). In addition, to allowcomparison with published data from other sigmo-dontines, and particularly from other oryzomyinetaxa, we calculated the distance values betweenpairwise taxa using Kimura’s two parameter (K2P)model (Kimura, 1980) for the cyt B gene.

The Markov Chain Monte Carlo (MCMC) methodwithin a Bayesian framework (hereafter BMCMC)was used to estimate the posterior probability ofphylogenetic trees. The MCMC procedure ensuresthat trees are sampled in proportion to their prob-abilities of occurrence under the model of gene-

Cytochrome b

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Figure 2. Nucleotide-based pairwise distances calculatedindependently for each gene (A, cytochrome b; B, NADH1),vs. pairwise distances calculated from the concatenation oftwo genes (see Material and methods for the calculation ofdistances).

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sequence evolution. Approximately 22 000 000phylogenetic trees were generated using the BMCMCprocedure, sampling every 1000 trees to ensure thatsuccessive samples were independent. The first 50trees of the sample were removed to avoid includingtrees sampled before convergence of the MarkovChain. A general likelihood-based mixture model(MM), based on the general time-reversible (GTR)model (see Rodríguez et al., 1990) of gene-sequenceevolution, was used to estimate the likelihood of eachtree, as described by Pagel & Meade (2004, 2005).This model accommodates cases in which differentsites in the alignment evolved in qualitatively distinctways, but does not require prior knowledge of thesepatterns or partitioning of the data. These analyseswere conducted using the software BayesPhylogenies,available from http://www.evolution.reading.ac.uk/BayesPhy.html. In order to find the best MM of gene-sequence evolution, we obtained the likelihood of thetrees by first using a simple GTR matrix, then usinga GTR matrix plus the gamma-distributed rate het-erogeneity model (1GTR + G), and then continuing toadd up to six GTR + G matrices. For the posterioranalyses, only the combination of matrices with thefewest number of parameters that significantlyincreased the likelihood was used, which was evalu-ated using a one-way ANOVA for balanced data setsin Statistica 6.0 (StatSoft Inc.), and then by a poste-rior Newman–Keuls test (Zar, 1996). Assumptions ofnormality of data and homogeneity of variance werepreviously evaluated. Posterior probabilities fortopologies were then assessed as the proportion oftrees sampled after burn-in, in which that particulartopology was observed.

As our results did not support the generalizedmolecular clock model (Likelihood Ratio = 74.34,d.f. = 17, P < 0.0001), we used a relaxed molecularclock by running BEAST v.1.4.8 (Drummond et al.,2006), which employs a BMCMC to co-estimate topol-ogy, substitution rates, and node ages. Posteriorprobability distributions of node ages were obtainedfor the concatenated two-gene alignment. TheGTR + G + I model with rate variation (six gammacategories) was implemented for the concatenatedgenes. The analysis implemented a Yule branchingrate prior, with rate variation across branchesasumed to be uncorrelated and lognormally distrib-uted (Drumond et al., 2006). The MCMC chain wasrun for 10 000 000 generations (burn-in 10 000 gen-erations), with parameters sampled every 1000 steps.Examination of MCMC samples using TRACER 1.4(Rambaut & Drummond, 2003) suggested that theindependent chains were each adequately samplingthe same probability distribution: effective samplesizes for all parameters of interest were greater than500.

We used two points of fossil calibration based onPardiñas, D’Elía & Ortiz (2002): C1, an O. flavescensfossil specimen from the Ensenadense level dated to amean time of 1.5 Mya; and C2, an O. eliurus fossilspecimen from the Lujanense level dated to a meantime of 0.24 Mya. As these datings do not have anassociated error, we used additional data reported bySchultz et al. (2004) for the Argentinean Pampa. Byusing radiometric 40Ar/39Ar, they dated a Pleistocenesite as 0.23 ± 0.03 Mya, which is equivalent to thestratus of the O. eliurus fossil. This error was incorpo-rated into the molecular clock analysis as part of theprior probability through a uniform distribution wherethe mean corresponded to the fossil age and the errorcorresponded to the radiometric error. We did notfind an error associated with C1; however, we used astandard deviation equivalent to half the Ensenadenselevel (1.5 ± 0.64 Mya). Thus, we used the fossil calibra-tion as an uncertain age, and the node age estimationwas set to normal distribution. With the former param-eters, we first estimated divergence at the root of thetree, then the in-group divergence, and finally thedivergence at several clades, as shown in Figure 3.

DISPERSAL–VICARIANCE ANALYSIS

To infer the history of biogeographic distributions inOligoryzomys, we used the known distributions ofeach species, as coded in the Appendix, optimized onthe combined-data tree using dispersal–vicarianceanalysis (DIVA 1.1; Ronquist, 1996, 1997). Thisprogram infers ancestral distributions based on athree-dimensional cost matrix derived from a simplebiogeographical model. The advantage of thisapproach is that it does not require a general a priorihypothesis of area relationships.

RESULTSNUCLEOTIDE VARIATION ANALYSES

The final alignments were 977 bp for the cyt B geneand 959 bp for the NADH1 gene, which provided acombined data matrix of 1936 characters. The overallbase composition for each gene was as follows: cyt B,A, 31%; C, 29%; T, 28%; and G, 12%; and NADH1, A,35%; C, 30%; T, 27%; and G, 8%.

The K2P distance for the cyt B gene (Table 2)exhibited values that ranged between 0.722% for speci-mens of the same locality, and 1.345% for specimens ofthe same species from different localities, such asisland and continent representatives (e.g. O. longicau-datus). However, the K2P distance values betweendifferent species varied between 5.7% (O.longicaudatus–Oligoryzomys fornesi [Massoia, 1973])to 15% (e.g. O. microtis–O. andinus). Other valuesbetween recognized Oligoryzomys species were about

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10% between the sister taxa O. fulvescens and O.vegetus, or about 6% between O. flavescens and O.destructor. The K2P distance values among represen-tatives of the same taxon (the unnamed Oligoryzomyssp. 1) were less than 1%, and the K2P distance betweenthe other unnamed species Oligoryzomys sp. B and itsclosest relative O. fornesi was 3.6% (Table 2).

PHYLOGENETIC ANALYSES

The two genes used in the present study are func-tionally independent, and exhibit unique evolutionarypatterns (Fig. 2). The rate of nucleotide substitutionfor each gene was relatively homogeneous across thelength of their sequences, but NADH1 has a muchhigher rate of substitution than cyt B. The predicteddistance values (Fig. 2C) show different slopes(t-Student = 12.48; d.f. = 169; P < 0.001), evidencingtwo evolutionary rates in the molecular markersanalysed. On the other hand, the partition homoge-neity test suggested that our data sets were notsignificantly incongruent (P = 0.01), following the cri-teria of Cunningham (1997). Therefore, these datawere combined for further phylogenetic analysis.

A similar topology was obtained with both the MPvia WP and BMCMC analyses. The WP resulted in asingle most parsimonious tree that was 2517 stepslong: consistency index, CI = 0.5217; retention index,RI = 0.6033. Of the total 1936 characters combining

both genes, 485 were parsimony informative. Both,WP and BMCMC (Fig. 3) showed the same topologyand hypothesized O. microtis as the most basal taxonwithin Oligoryzomys, with 100% bootstrap and 1.00posterior probability support, respectively (Fig. 3).The WP and BMCMC trees exhibit a split that recov-ered a well-supported clade (1.00 and 100) thatincluded (((O. fornesi, Oligoryzomys sp. B), O.andinus), O. longicaudatus) on one clade, and all ofthe other species of Oligoryzomys on the other clade.In the latter clade we recovered a split between twomajor groupings: (O. fulvescens, O. vegetus) on oneside, and a major clade that included ((O. delticola, O.eliurus), O. chacoensis) in a sister relationship with aclade that included (((O. flavescens, O. destructor),Oligoryzomys sp. 1), O. nigripes).

Age estimations from the relaxed clock analysisestimated 6.67 ± 0.02 Mya for the divergence betweenOligoryzomys with respect to the out-groups, and5.27 ± 0.052 Mya for the split between O. microtisand the rest of the species (Fig. 3). Other age estima-tions were as follows: 2.2 ± 0.043 Mya for clade 1 (((O.fornesi, Oligoryzomys sp. B), O. andinus), O. longi-caudatus); 3.35 ± 0.035 Mya for clade 2 (O. fulvescens,O. vegetus); 3.71 ± 0.035 Mya for clade 3, composed ofclade 4 ((O. eliurus, O. delticola), O. chacoensis) andclade 5 O. nigripes; and 1.54 ± 0.031 Mya for clade 6,composed of (((O. destructor, O. flavescens), Oligory-zomys sp. 1).

sp1 MIC210sp1 MIC203

sp1 MIC211

O.destructor NK22846

1

4

3

5

6C1

C2

2

O.O.

O.

1

4

3

5

6C1

C2

2

O.flavescens NK21532

O.nigripes GD547O.delticola GD569

O.eliurus NK42266O.chacoensis NK72388

O.fulvescens NK101588

O.vegetus KU142065O.fornesi GD259O. spB 3203MUSA2625

O.andinus BOLNK11547O.longicaudatus BIJCT1960

O.longicaudatus NK95245O.microtis NK13425

Transandinomys talamancaeHolochilus brasiliensis

1.001000.99

890.8564

1.00100

0.80

1.00

700.6483

1.00100

1.00100

1

4

3

5

6C1

C2

2

0.1

1.00100

1.0099

1.00100

1

4

3

5

6C1

C2

2

Figure 3. Oligoryzomys phylogeny based on weighted parsimony analysis (WP) and the Bayesian Markov Chain MonteCarlo method (BMCMC). The phylogeny was obtained for the combined mitochondrial cytochrome b and NADH1 sequencedata, whereas BMCMC represents a consensus tree of the N = 21 950 trees from the converged Markov chain. A posteriorprobability above 0.5 and bootstrap values over 50% are represented on each node. C1 represents calibration time1 = 1.5 Mya; C2 represents calibration time 2 = 0.24 Mya (according to Pardiñas et al., 2002; see Material and methods).Diamonds on nodes represent that clade number for the clock calibration using BEAST.

558 R. E. PALMA ET AL.

© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 160, 551–566

Tab

le2.

Kim

ura’

stw

opa

ram

eter

(K2P

)m

odel

dist

ance

valu

esam

ong

pair

-wis

eO

ligo

ryzo

mys

spp.

for

cyto

chro

me

bse

quen

ces

Taxo

nna

me

12

34

56

78

910

1112

1314

1516

1718

19

1O

.fo

rnes

iG

D25

9–

2O

ligo

ryzo

mys

spB

.32

03M

USA

2625

0.03

7–

3O

.an

dinu

sN

K11

547

0.06

70.

070

–4

O.

long

icau

datu

sB

IJC

T19

600.

079

0.05

50.

083

–

5O

.lo

ngic

auda

tus

NK

9524

50.

057

0.05

80.

082

0.01

3–

6O

.ni

grip

esG

D54

70.

098

0.09

20.

124

0.08

30.

089

–7

O.

delt

icol

aG

D56

90.

094

0.09

10.

120

0.07

90.

085

0.00

9–

8O

.el

iuru

sN

K42

266

0.09

60.

094

0.11

20.

079

0.08

70.

030

0.03

2–

9O

.ch

acoe

nsis

NK

7238

80.

098

0.09

90.

116

0.08

50.

091

0.11

30.

113

0.10

4–

10O

.fu

lves

cens

NK

1015

880.

096

0.09

50.

119

0.09

60.

097

0.10

70.

108

0.10

10.

108

–

11O

.ve

getu

sK

U14

2065

0.11

80.

116

0.13

30.

110

0.11

10.

108

0.11

10.

114

0.11

50.

101

–12

Oli

gory

zom

yssp

.1

MIC

210

0.11

10.

109

0.11

90.

112

0.10

90.

110

0.10

90.

105

0.10

60.

110

0.09

9–

13O

ligo

ryzo

mys

sp.

1M

IC20

30.

105

0.10

30.

116

0.11

30.

111

0.11

10.

110

0.10

70.

108

0.10

80.

103

0.01

0–

14O

ligo

ryzo

mys

sp.

1M

IC21

10.

111

0.10

90.

117

0.11

20.

109

0.11

00.

109

0.10

40.

100

0.10

90.

103

0.00

70.

009

–

15O

.fla

vesc

ens

NK

2153

20.

130

0.12

80.

132

0.12

80.

129

0.13

30.

132

0.12

30.

106

0.12

20.

121

0.05

70.

060

0.05

0–

16O

.de

stru

ctor

NK

2284

60.

146

0.14

20.

150

0.14

50.

143

0.14

00.

138

0.13

20.

135

0.13

40.

145

0.09

80.

101

0.09

40.

063

–17

O.

mic

roti

sN

K13

425

0.14

60.

138

0.15

10.

138

0.14

0.13

60.

137

0.13

40.

136

0.14

40.

138

0.10

20.

107

0.09

80.

090

0.10

8–

18Tr

ansa

ndin

omys

0.12

30.

113

0.13

80.

106

0.10

40.

138

0.13

50.

129

0.11

80.

114

0.12

70.

124

0.12

70.

127

0.14

50.

153

0.14

4–

19H

oloc

hilu

s0.

159

0.15

30.

155

0.15

20.

152

0.17

40.

172

0.16

40.

172

0.17

30.

191

0.18

70.

184

0.18

40.

188

0.21

40.

207

0.18

9–

PHYLOGENY OF OLIGORYZOMYS 559

© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 160, 551–566

DIVA ANALYSIS

Optimization of geographic distributions of taxa usingdispersal/vicariance analysis (Fig. 4) revealed thebasal clade (constituted by O. microtis) to be from theAmazonian, Cerrado, and Chaco ecoregions of SouthAmerica. The next succesive basal clade, clade 1, isfrom the highlands of the Andes and Patagonia; clade2 is from the Pacific Province; clades 3, 4, and 5 arefrom the Cerrado; whereas clade 6 is from theCerrado and Yungas (see Fig. 4).

DISCUSSIONPHYLOGENETIC ANALYSES AND NUCLEOTIDE

VARIATION

Both WP and Bayesian analyses recovered O. microtisas the most basal taxon in the evolution of the genusOligoryzomys. A similar conclusion was reached byRivera et al. (2007), as well as by Miranda et al.(2008): Miranda et al. (2008) based their study on cytB sequences that included some of the species consid-ered in this study. Except for O. microtis forming itsown group and the sister relationship of O. fulvescensand O. vegetus, we did not recover any other speciesgroups proposed by Carleton & Musser (1989). One ofthe well-supported clades obtained in our study (((O.fornesi, Oligoryzomys sp. B), O. andinus), O. longi-caudatus) was supported by the phylogeny of Myerset al. (1995), based on partial cyt B sequences: theyfound that O. fornesi was more closely related to O.longicaudatus, and not to O. microtis as had beenhypothesized by Carleton & Musser (1989) based onmorphology. The inclusion of O. andinus in this cladedoes not agree with Myers et al. (1995), who recovered

this species as sister to O. microtis. However, highbootstrap support and posterior probability valuesmakes the hypothesized (((O. fornesi, Oligoryzomyssp. B), O. andinus), O. longicaudatus) clade obtainedin our study more likely. Oligoryzomys sp. B (sensuCarleton & Musser, 1989) should be treated carefully,as this taxon was included in the flavescens group byCarleton & Musser (1989). The latter authors pro-posed that Oligoryzomys sp. B could be the Andeancounterpart of O. flavescens, as the former is distrib-uted above 2000 m a.s.l. in the central Andes. Carle-ton & Musser (1989) reported Oligoryzomys sp. Bfrom the eastern Puna and Amazon slopes of theAndes, and from the Pacific side of the southernPeruvian Andes between 3000 and 4000 m a.s.l. Thespecimen of Oligoryzomys sp. B analysed by us wastrapped in Limbani, Puno department, Peru, whichwas one of the collecting localities reported for thistaxon by Carleton & Musser (1989). However, theOligoryzomys sp. B analysed by us was recovered assister to O. fornesi from the Chaco region, and ishighly divergent with respect to O. flavescens. Indeed,the K2P distance value between sister taxa Oligory-zomys sp. B and O. fornesi was 3.7% for the cyt Bgene, whereas the K2P cyt B distance value betweenOligoryzomys sp. B and O. flavescens was 12.7%. TheK2P value (3.7%) obtained for Oligoryzomys sp. Bwith respect to O. fornesi represents nearly a half orone-third of the nucleotide distance value obtainedbetween well-recognized species (Steppan, 1998;Smith & Patton, 1999; Palma, Marquet & Boric-Bargetto, 2005a; this study, e.g. O. andinus–O. longi-caudatus, O. vegetus–O. fulvescens), suggesting thatOligoryzomys sp. B might be speciating. This inter-

O.sp1O.flavescensO.destructorO.nigripesO.delticolaO.eliurusO.chacoensisO.fulvescensO.vegetusO.fornesiO.spBO.andinusO.longicaudatusO.microtis

1

3

4

5

6Cerrado - Yungas

Cerrado

Cerrado

Cerrado

Pacific Province

Andean – Patagonia O

AmazonianCerradoChaco

Andean – Cerrado 2

1

3

4

5

6

O

2

Figure 4. Dispersal–vicariance analysis with geographic regions optimized onto the topology of the Bayesian consensustree. The hypothetical ancestral distributions obtained through this method are listed above the branches.

560 R. E. PALMA ET AL.

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pretation agrees with previous work in other sigmo-dontine taxa (e.g. Oryzomyini and Phyllotini) thatdemonstrated a genetic distance between subspeciesof rodents in a range that varied by less than 4%(Myers et al., 1995; Steppan, 1998). Oligoryzomysandinus, on the other hand, appeared as sister to the(O. fornesi, Oligoryzomys sp. B) union, contrary to therelationship with O. chacoensis proposed by Carleton& Musser (1989). Finally, the basal part of the formerclade recovered both O. longicaudatus specimens –one from Navarino Island (54°S) and the other fromCoyhaique (45°S) on the continent – as having a 1%K2P distance value. This slight nucleotide differencebetween the insular and continental representativesof O. longicaudatus confirms previous results aboutthe strong genetic/molecular homogeneity of thisspecies along its wide distributional range in thesouthern Andes (Gallardo & Palma, 1990; Palmaet al., 2005b).

Another well-supported relationship was thatbetween Oligoryzomys sp. 1 and its closest relativesO. flavescens and O. destructor. These samples werecollected in Catamarca Province, north-west Argen-tina. Cranial and dental morphology supported dif-ferences with related species, although a name hasyet to be assigned (M.I. Carma unpubl. data). Ourmolecular analyses supported the validity of thisnew taxon, and the individuals studied seem to con-stitute a valid species when contrasted with theirsister taxa O. flavescens and O. destructor. The K2Pdistance value for the cyt B gene between Oligory-zomys sp. 1 and O. flavescens varied around 6.0%,whereas the distance between Oligoryzomys sp. 1and O. destructor was about 10% for the same gene.This new taxon (Oligoryzomys sp. 1) is probably anoffshoot of one of these two latter taxa, most likely aperipheral isolate of O. flavescens, as the southerndistributional limit of O. destructor seems to be Chu-quisaca, in Bolivia (Carleton & Musser 1989). In thelast species account, Musser & Carleton (2005)included a new species of Oligoryzomys, O. brendae,as distributed from Tucuman and Catamarca. TheOligoryzomys sp. 1 representatives in this study arefrom Catamarca in the north-west of Argentina. Weare not sure if the Oligoryzomys sp. 1 reported by usin this study is the same O. brendae presented inMusser & Carleton (2005), as no formal descriptionfor O. brendae is yet available (the citation inMusser and Carleton refers to a meeting presenta-tion), and hence this name as published constitutesa nomen nudum.

The phylogenetic relatedness of O. vegetus and O.fulvescens with respect to other Oligoryzomys spp. iswell supported in both phylogenetic analyses. Bothoptimality criteria recovered these two species assister taxa. The close relationship between these two

species seems plausible, given their biogeographicrelatedness in Central America and the morphologicalcharacteristics that relate both taxa together with O.arenalis in the fulvescens group (Carleton & Musser1989).

The next clade in the WP and Bayesian tree recov-ered O. delticola and O. eliurus in a sister relation-ship, and as being closely related to O. chacoensis asa first out-group. The first two taxa together with O.nigripes and O. longicaudatus are part of the nigripesspecies group sensu Carleton & Musser (1989). Ourmolecular mitochondrial results give no support forthe nigripes species group, particularly with regardsto the inclusion of O. nigripes, O. longicaudatus, andO. destructor. According to our results, the unionbetween O. eliurus and O. delticola exhibits shortbranch lengths in the WP and BMCMC total evidencetree, and the K2P distance value for the cyt B genebetween these two species is low (~3%), a value closeto that obtained for subspecies in other related sig-modontine taxa (Steppan, 1998; Smith & Patton,1999; Palma et al., 2005a; this study). We obtainedstrong support for the relationship between O. delti-cola and O. eliurus, and other studies have proposedO. delticola to be a junior synonym of O. nigripes(Bonvicino & Weksler, 1998; Francés & D’Elía, 2006),based on karyotypes and GTG-banding similarities.Further work based on morphology and chromosomeshave stated that it is difficult to separate O. delticolaand O. eliurus from O. nigripes (Weksler & Bonvicino,2005), and more recently Paresque et al. (2007) pro-posed leaving O. delticola and O. eliurus as juniorsynonyms of O. nigripes. Our results, however,showed O. nigripes as part of a different clade, com-pared with O. delticola and O. eliurus, with a mod-erate support in both the WP and BMCMC analyses(Fig. 3). Based on our results, we believe that O.nigripes is a different species with respect to O.eliurus and O. delticola, and that these two taxa couldconstitute the same species.

BIOGEOGRAPHY

The fossil record of oryzomyines is poor. The earliestrecords from South America are from the Pleistocene(Steppan, 1998; Pardiñas et al., 2002). According tomolecular evidence, the hypothesized time of arrivalof sigmodontines in South America was prior to theformation of the Panamanian land bridge, and wasachieved by waif dispersal via island hoping and/orrafting (Steppan et al., 2004; Smith & Patton, 2007).The occurrence of oryzomyine forms in Central andNorth America must be a back dispersal from thesouth, probably as part of, or as a by-product of, theGreat American Interchange (Simpson, 1980) onceNorth and South America were connected via CentralAmerica.

PHYLOGENY OF OLIGORYZOMYS 561

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Oligoryzomys (together with Zygodontomys,another component of the oryzomyine radiation) isone of the oryzomyines that does not have a knownpattern of geographic distribution (Weksler, 2006). Intrying to explain the patterns of geographic distribu-tion for oryzomyines in the Neotropics, Weksler(2006) found that most species of oryzomyines fol-lowed a trans-Andean (west to the Andes) or cis-Andean (east to the Andes) distribution, or occurredin the Andes as a whole. However, this pattern doesnot fit Oligoryzomys, as this genus ranges fromMexico to Patagonia.

The position of O. microtis at the base of Oligory-zomys radiation supports earlier claims that theorigin of the genus (and the tribe for that matter)should be localized in the premontane forests of thenorthern Andes Mountains or the western Amazonlowland forests (Reig, 1986; Weksler, 2006). Thishypothesis was independently proposed by Reig(1986) based on the number of taxa found in thenorthern Andes Mountains (Ecuador, Colombia, andVenezuela). Reig (1986) recognized 14 species of ory-zomyines in that area, five of which were endemic.Twenty years later, Weksler (2006) proposed the pre-montane forests of the northern Andes Mountainsand the western Amazon lowland forests as two can-didate places for the probable centre of origin oforyzomyines. Our results suggest that the Amazonlowlands, the Cerrado, and the Chaco are the mostparsimonious areas of origin, which partially agreeswith Weksler (2006) and mostly agrees with Mirandaet al. (2008). Our molecular clock estimates havehypothesized a time of 6.67 Mya for the differentia-tion of Oligoryzomys spp., which falls within the timerange given for the initial diversification of oryzomy-ines (between 5 and 9 Mya). This date has beenproposed by Smith & Patton (1999), based on cyt Bsequences, and by Steppan et al. (2004), based on fournuclear genes. The hypothesized time of origin for thegenus corresponds to the end of Miocene (and evenearlier than that, see Steppan et al., 2004), and isabout the time suggested for the probable arrival ofearly sigmodontines in South America (Spotorno,1986; Smith & Patton, 1999; Steppan et al., 2004).From a biogeographic perspective, that period wascharacterized by the formation of a vast array ofhabitats, not only for oryzomyines, but also for theradiation of sigmodontines in general. This was atime when forests and woodlands (subtropical andtemperate) covered most of the continent (Hinojosa &Villagrán, 2005). Increasing orogenic events associ-ated with the rising of the Andes Mountains resultedin a gradual cooling and drying, which increased thespread of woodlands and savannas, and the contrac-tion of forests (Potts & Behrensmeyer, 1992; Garzioneet al., 2008). In addition, our molecular clock calibra-

tion hypothesized two other major pulses for theradiation of Oligoryzomys: the first being about 3.7–3.0 Mya, which allowed the diversification of thespecies in clade 3 (Fig. 3). The second major pulse wasthe diversification of forms included in clades 1 and 6,between 2.2 and 1.5 Mya. The latter diversificationrate corresponded to a period of alternating intergla-cial and glacial events in the Pleistocene (Holling &Schilling, 1981). Thus, the timing obtained throughmolecular clock calibration for Oligoryzomys spp.placed this taxon in a scenario of strong habitatchange on the continent that may have promoted thedifferentiation of several taxa.

The recent work by Miranda et al. (2008) proposeda north-to-south gradient of dispersal for the differentspecies of Oligoryzomys in South America, first occu-pying the Amazon and the Cerrado ecogeographiczones. Our results do not allow us to verify thisnorth-to-south gradient, although we agree that theAmazon and the Cerrado must be the ancestral areafor the radiation of Oligoryzomys. We thus suggestthat the radiation of Oligoryzomys occurred in fourareas stemming from a widely distributed ancestralform such as O. microtis. These included the followinggroups.

1. An Andean–Chacoean group including O. fornesi,Oligoryzomys sp. B, O. andinus, and O. longicau-datus, with an estimated diversification time ofabout 2.2 Mya from an Andean Patagonian ances-tral distribution (Fig. 4). This diversification leftOligoryzomys sp. B and O. andinus in the high-lands of the central Andes, O. fornesi in the foot-hills of the Andes and part of the Chaco region,and O. longicaudatus in the southern lowlandsthat ranges from the Andes Mountains of Argen-tina and Chile southwards to Patagonia.

2. A group that relates O. flavescens from part of theChaco, the Monte Desert, and the east–centralportion of Argentina with O. destructor from thewest–central Amazonia, and south to subtropicalareas of Paraguay and Argentina. This clade gaverise to a new species, Oligoryzomys sp. 1, in thenorth-western portion of Argentina that could be anoffshoot of O. flavescens. At the base of this radia-tion is O. nigripes, which occurs in northern Argen-tina (Formosa and Misiones provinces) and east ofthe Paraguay River. This radiation originated froman ancestor-form inhabitant of the Cerrado.

3. A group closely associated with group 4, a cladecontaining O. eliurus from the Brazilian Caatingaand Cerrado, and O. delticola from Uruguay andthe delta of Paraná River. Basal to this relationshipis O. chacoensis from the Chaco, Cerrado, andCaatinga of Brazil. All these forms originated froma Cerrado ancestor.

562 R. E. PALMA ET AL.

© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 160, 551–566

4. Finally, O. fulvescens was recovered as a sistertaxon to O. vegetus, which occurs in Central andsouthern North America, and may be a southerninvader to the north, after the re-establishment ofthe Panamanian bridge by Plio–Pleistocene times,once the bridge between Central and South Americawas re-established (Simpson, 1980). In fact, timecalibration for the split between O. fulvescens andits sister taxon O. vegetus gave a diversification ofabout 3.35 Mya, a time where the bridge betweenboth continents was already set. Oligoryzomysvegetus, on the other hand, could be a peripheralisolate of O. fulvescens.

ACKNOWLEDGEMENTS

This work is dedicated to the memory of Terry L.Yates who died while performing this work. We appre-ciate the comments of Jennifer K. Frey who helped toimprove this manuscript, and the laboratory supportfrom Dusan Boric-Bargetto. We thank Juan CarlosTorres-Mura for the loan of specimens from NavarinoIsland. We thank the following for loans of tissuesamples and specimens: Guillermo D’Elía, BlasArmien, Enrique Lessa, the Museum of SouthwesternBiology, University of New Mexico, and the Univer-sity of Kansas Museum of Natural History. This workwas supported by grants NIH-Hantavirus Chile andPanamá, FONDAP-CASEB 1501-0001 Programa 2,DIUC 205.113.070-1.0, FONDECYT 1990156, FOND-ECYT 3050092, and FONDECYT 1070331. The col-lecting permits of Servicio Agricola Ganadero (SAG)and Corporación Nacional Forestal from Chile arealso acknowledged.

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APPENDIX

Ecogeographic zones of distribution for the Oligoryzomys spp. used in the DIVA analysis

Species Ecogeographic zones of distribution

Oligoryzomys andinus Sechura desert; Central Andean wet puna; Bolivian Yungas1

Oligoryzomys chacoensis Chaco; Chiquitano dry forests; Cerrado1

Oligoryzomys delticola Humid pampas; Uruguayan savanna1,2,3,4,5

Oligoryzomys destructor Napo moist forests; Ucayali moist forests; Bolivian Yungas1

Oligoryzomys eliurus Cerrado; Caatinga; Atlantic rainforests1,5

Oligoryzomys flavescens Humid chaco; Uruguayan savanna; humid pampas; Argentine espinal; Argentine monte;Cerrado; Caatinga; Atlantic rainforests1

Oligoryzomys fornesi Humid chaco; Cerrado; Caatinga; Atlantic rainforests1,2,6

Oligoryzomys fulvescens Moist forests of west and east versants of south Mexico; Llanos; Moist forests ofGuiana and northernmost Brazil1,7,8

Oligoryzomys longicaudatus Chilean matorral; Valdivian rainforests; Magellanic subpolar forests; Patagoniansteppe9,10

Oligoryzomys microtis Amazon forests of Brazil, Perú, and Bolivia; Humid Chaco1,5

Oligoryzomys nigripes Humid Chaco; Cerrado; Caatinga; Atlantic rainforests1,4,5

Oligoryzomys vegetus Lower montane and montane forests of Costa Rica and Panamá1

Oligoryzomys sp. 1 Southern Andean Yungas1

Oligoryzomys sp. B Altoandina11

1Musser & Carleton (2005); 2Myers & Carleton (1981); 3Espinosa & Reig (1991); 4Bonvicino & Weksler (1998); 5Andrades-Miranda et al. (2001); 6Lacher & Alho (2001); 7Gardner & Patton (1976); 8Haiduk, Bickham & Schmidly (1979); 9Palmaet al. (2005a); 10Belmar-Lucero et al. (2009); 11Carleton & Musser (1989).

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